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Vascular Remodelling

E. Gautier I, B.A. Rahn 2, S.M. Pen-en 2

1 Department of Orthopaedic Surgery, University of Beme, Inselspital, CH-3010 Beme, Switzerland 2 AO/ASIF Research Institute, Clavadelerstrasse, CH-7270 Davos

Summary’

It is well known that in a plated bone segment, bone loss can be observed radiologically and histologically. The former explanation of this phenomenon was based on Wolff’s law which explains changes in bone mass and structure in terms of the functional demands of the skeleton. More recent studies have shown that this bone loss as seen near the implant in the early phase after internal fixation is not induced by stress protection (unloading). Porosis is a temporary stage of intense remodelling and is related to the vascular damage produced by the implantation and by the presence of the implant. Early temporary bone loss and remodelling is not only seen after plating but also around pins and screws and even more extensively after intramedullary nailing. Refractures after implant removal seem to be related to the slow healing potency of the disturbed cortex directly beneath the plate and the consequent stress riser effect. The first stage of healing under the plate consists of the revascularization and revitalization of the dead bone cortex by Haversian (intracortical) or pericortical remodelling. The innovative concept behind recently designed plates is the improvement of the blood supply near the implant, the maintenance of an optimal bone structure in the vicinity of the plate and improved healing in the critical zone without additional implant-related damage.

Keywords: Vascularity, blood supply, necrosis, porosis, remodelling, plate fixation.

Vascularity and healing of bone

The afferent blood supply to the bone consists of three main components: the principal nutrient artery, the metaphyseal vessels, and the periosteal arteries. The intramedullary system is the major afferent supply nourishing the inner two thirds of the bone cortex. The periosteal vessels enter the cortex mainly at sites of fascial and muscle attachment and appear to supply the outer third of the bone diaphysis (l-7).

The periosteum has a rich vascular network (8). For bone perfusion, the periosteal supply of blood is less important than the venous drainage because blood flow through the cortex is predominantly centrifugal (9-11). Following trauma or operation with damage to the intramedullary vessels, a compensatory flow reversal is observed.

The most critical prerequisite for sound bone healing is the unimpaired viability of the bone tissue. Avascular bone fragments prevent callus bridging of the fracture gaps. Regardless of the state of reduction and stability, dead bone only heals once the necrotic areas have been revascularized (Fig. la-d).

1 Abstracts in German, French, Italian, Spanish and Japanese are printed at the end of thik sutiplement.

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Functional adaptation of bone

Fig. la and b: Anteroposterior and lateral view of a II” open fracture of the femur in a 20-year-old patient following a motorbike accident.

The adaptation of bone tissue to functional load is a well known phenomenon. In the 19th century, this theory was postulated for cancellous bone and has now found acceptance as Wolff’s Law (12-15). Later it was expanded to include cortical bone (16-20). The strain within the bone tissue varies around 1000 microstrain under normal daily loading conditions. An increase in the tissue strain results in bone deposition whereas a decrease results in bone resorption (21). The peak strains are approximately 2000 - 3000 microstrains and the strain at the fracture lies at 20’000 microstrains (2%) which indicates extreme tolerance of impact (22).

Bone reaction to implants

Bone activity such as resorption and formation rely upon an intact blood supply to the bone. The specific reason underlying the remodelling process cannot be deduced from the bone response. Histologically, the remodelling observed during the revascularization of necrotic bone is identical to that which occurs in direct fracture healing. In addition, unspecific reactions of the inner and outer bone shell to trauma, operation and to the implant can be observed radiologically and histologically.

Experimentally, bone atrophy or porosis is seen in the segment of the diaphysis to which a plate is applied. The common explanation has been that this might be due to the mechanical unloading of the plated bone segment based on Wolff’s Law. However, there are various bone responses to plating which cannot all be explained by the changes in loading conditions. Changes in the bone structure such as cortical porosity due to internal remodelling or changes in the bone mineral content have been described. A decrease in the bone cross sectional area due to bone resorption on the inner or outer surface of the cortex also has been observed (23-32). The reversibility of the structural alterations of the bone only after implant removal has been observed by some authors (23, 28, 33, 34) and the same process with the implant still in place by others (35-38).

Fig. lc and d: 10 and 18 weeks after intramedullary nailing, a partial necrosis of the proximal fragment end with relative hyperdensity was visible. The necrosis was slowly revascularized. The remodelling of the cortex radiologically is discernible by the concomitant temporary porosis. Callus formation and thus healing in this case takes place only in areas with undisturbed bone viability.

The use of less rigid plates has been recommended as a method of decreasing intracortical porosity (32, 39- 41). A less pronounced cortical thinning with more flexible plates has also been reported in the literature (34,42).

Other studies reveal vascular damage to the bone near the plate (43-48). This is apparent not only beneath the’ plate but also in the vicinity of more or less any

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implant used in orthopaedic surgery, such as mtramedullary nails, screws and pins (49-54).

Problem of refracture after internal fixation

The clinical importance of the structural changes of the bone in the plated segment is understood in terms of the decrease in strength and stiffness. When the implant is removed, the bone has not yet reached its prefracture strength and therefore there is a certain danger of refracture. The term “stress protection” is often used to describe this mechanically adverse side effect of plate fixation (55-58). In the literature, other explanations for refracture can be found, such as too early implant removal, incomplete consolidation of the fracture, stress riser effect of the screw holes, and disturbed fragment vitality (56-63).

Postoperatively, the structural alterations and the degree of consolidation of the cortex beneath the plate are often obscured by the implant and thus, remain invisible. Only after implant removal can the extent of the persistent remodelling be detected. Correct radiographic technique permitting a clear view of the cortex adjacent to the plate is essential if continuing bone remodelling is to be correctly assessed (Fig. 2a-e).

Fig. 2a and b: Closed forearm fracture in a 23-year-old patient stabilized by means of two 3.5 mm dynamic compression plates.

Fig. 2c and d: At 4 years after the operation, the radiography shows healing of both bones. But the cortex directly underneath the plate is not completely visualized to assess the degree of remodelhng in this critical area. The intense remodelling activity still in progress in the cortex underlying the plate only becomes visible at implant removal.

Fig. 2e: Enlargement of the critical area with intense remodelling still in progress.

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Assessment of the bone reaction after plating

Materials and methods

To assess the effect of plate stiffness on blood supply, remodelling and porosis, a study was undertaken on sheep. The intact tibiae were plated: in one group conventional metal plates were used, in the other experimental plates made of polyacetal with a metal core. Keeping screw torque values constant, the amount of plate contact was assessed during surgery with a special contact bag. At four weeks, the disturbance to the blood supply both in the plate bed and intracortically in bone cross sections was quantified by the preterminal administration of disulphine blue. Bone remodelling was assessed during the whole experimental period using polychrome fluorescent labelling of the bone. Porosity was measured at four, ten and twenty weeks after surgery using an automatized computer digitizer system.

Results

At four weeks, a large area of non perfused periosteum was seen in the plate bed. On cross sections, large areas of perfusion deficiency varying in depth and width were seen (Fig. 3a-h). The intracortical lack of perfusion is related to the amount of bone-to-plate contact and consequent destruction of the periosteal vascular network. Outside the plated segment, bone perfusion remains undisturbed. The more flexible polyacetal plate caused more vascular disturbance because it adapted. easily to the bone surface when the screws were tightened. The disturbance of the blood supply resulted in an area of bone necrosis which was visible in Fuchsin stained specimens.

Ten weeks after the operation at the boundary between perfused and non perfused bone, resorption cavities contributing to temporary intracortical porosis were observed histologically. Later, they were filled with newly deposited bone lamellae.

The interdependence of temporary porosity of the bone cortex and Haversian remodelling can be demonstrated using the development of a single osteon as an example. First, the resorption lacunae appear, their diameter being decreased by centripetal bone deposition. In the end, the canal for the central vessels with a diameter of 30 to 50 micrometer persists (Fig. 4a-f).

Fig. 3a: Plate contact (plastic plate) at implantation as measured with the contact bag. The device indicates contact when the distance between plate undersurface and bone surface is less then 40 micrometers. Due to the geometrical properties of the plate and the bone in the proximal tibia, more cant; Ict was observed distally.

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Fig. 3b and c: Disturbance of the blood supply in the plate bed at explantation 4 weeks after surgery. Staining with disulphine blue represented schematically.

Gautier: Vascular remodelling

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I I

Fig. 3d - h: Perfusion deficiency intracortically at 4 weeks after the operation. The amount of mtracortical disturbance of the blood supply is related to plate contact and the associated destruction of the pe- riosteal vessels. Proximally, bone necrosis is more ex- tensive than distally. The site of the histological sec- tion from proximal to distal is indicated by markers on figures a and c.

Fig. 4a: Two single osteons remodelled within the 20 weeks experimental period. Bone deposition can be defined with the aid of fluorescent dyes administered weekly. During the 2nd month xylenol orange, during the 3rd month calcem green, the 4th alizarin complex- one and the 5th tetracycline labelling was used.

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Fig. 4b - f: Schematic representation of the same two osteons showing the amount of porosity and bone deposition at monthly intervals (from top to bottom: at 1,2,3,4, and 5 months).

At 20 weeks remodelling has taken place in the area of bone cortex in which the blood supply had been disturbed. The activity of remodelling always starts in the perfused zone and spreads towards the implant. The remodellmg revascularizes and revitalizes the necrotic bone. Depending on the access for bone remodelling cells (osteoclasts), the intracortical or supplementary pericortical reconstitution of the bone cortex is visible. With the plate in close contact to the bone, only intracortical activity is possible, nonetheless, at the plate boundaries pericortical osteoclastic activity followed by bone deposition can also be observed. The former leads to a decrease of the plate-bone contact area (Fig. 5a-o).

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Consistent with the amount of disturbed perfusion under plastic plates, the extent of bone remodelling and concomitant temporary porosis of the cortex is more pronounced than for steel plates.

Fig. 5a: Plate contact (steel plate) at implantation.

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Fig. 5d - h: Extent of intracortical and pericortical remodelling on cross sections. In those sections corresponding to high plate contact and consequent vascular disturbance, the area of intracortical remodelling is also more extensive. The sections were taken between the screws from proximally to distally.

Fig. 5b and c: Plate bed at explantation at 20 weeks after surgery. The disulphine blue staining indicates undisturbed vascularity at the periosteal surface. A tremendous decrease of plate contact can be observed compared to the initial situation at implantation of the plate.

Fig. 5i and k: Cross section at 20 weeks. The combination of mtracortical and pericortical remodelling can be seen. The latter leading to the decrease in plate contact.

Modifications of the plate undersurface with limited contact reveal the possibility of preserving bone viability under a plate by leaving the periosteum more or less undisturbed (38,64,65). The LC-DCP which is currently in clinical use is the first implant modified to preserve the bone circulation (66). In conventional plates load transmission is based on friction at the bone implant interface. Using such plates further reduction of the plate bone contact is limited by the compressive strength of cortical bone. With the PC- Fix, the load transmission is based on the interlocking of the screw heads in the plate holes. Thus, the amount of contact of the implant remains uncritical and without any adverse mechanical effects on the underlying bone.

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Fig. 51- o: Schematic representation of the pericortical remodelling in more detail. First the bone cortex is resorbed by osteoclastic activity on the periosteal envelope. Gradual bone deposition was observed during the 3rd, 4th and 5th month after. intervention.

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